Differential regulation of CaMKIIα interactions with mGluR5 and NMDA receptors by Ca2+ in neurons

Journal of Neurochemistry

Volumn 127, Issue 5, 2013, Pages 620-631

  Jin, Dao Zhong ^a   Guo, Ming Lei ^a   Xue, Bing ^a   Mao, Li Min ^a   Wang, John Q ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY SCHOOL OF MEDICINE   (United States)

Author keywords

calmodulin; GluN2B; mGluR; NR2B; nucleus accumbens; striatum

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II ALPHA; CALCIUM ION; METABOTROPIC RECEPTOR 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM CELL LEVEL; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME INHIBITION; IN VITRO STUDY; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RAT; RECEPTOR BINDING; SYNAPSE;

MAMMALIA; RATTUS;

CALMODULIN; GLUN2B; MGLUR; NR2B; NUCLEUS ACCUMBENS; STRIATUM;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CALMODULIN; CARRIER PROTEINS; CORPUS STRIATUM; MALE; MOLECULAR SEQUENCE DATA; NEURONS; NUCLEUS ACCUMBENS; PHOSPHORYLATION; RATS; RATS, WISTAR; RECEPTOR, METABOTROPIC GLUTAMATE 5; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION;

EID: 84887607467     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12434     Document Type: Article

References (49)

1. Attucci S., Carla V., Mannaioni G., and, Moroni F., (2001) Activation of type 5 metabotropic glutamate receptors enhances NMDA responses in mice cortical wedges. Br. J. Pharmacol. 132, 799-806.
2. Awad H., Hubert G. W., Smith Y., Levey A. I., and, Conn P. J., (2000) Activation of metabotropic glutamate receptor 5 has direct excitatory effects and potentiates NMDA receptor currents in neurons of the subthalamic nucleus. J. Neurosci. 20, 7871-7879.
3. Bard L., and, Groc L., (2011) Glutamate receptor dynamics and protein interaction: lessons from the NMDA receptor. Mol. Cell. Neurosci. 48, 298-307.
4. Bayer K. U., LeBel E., McDonald G. L., O'Leary H., Schulman H., and, Koninck P. D., (2006) Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B. J. Neurosci. 26, 1164-1174.
5. Benquet P., Gee C. E., and, Gerber U., (2002) Two distinct signaling pathways upregulate NMDA receptor responses via two distinct metabotropic glutamate receptor subtypes. J. Neurosci. 22, 9679-9686.
6. Bonsi P., Platania P., Martella G., Madeo G., Vita D., Tassone A., Bernardi G., and, Pisani A., (2008) Distinct roles of group I mGlu receptors in striatal function. Neuropharmacology 55, 392-395.
7. Choe E. S., and, Wang J. Q., (2001) Group I metabotropic glutamate receptors control phosphorylation of CREB, Elk-1 and ERK via a CaMKII-dependent pathway in rat striatum. Neurosci. Lett. 313, 129-132.
8. Choi K. Y., Chung S., and, Roche K. W., (2011) Differential binding of calmodulin to group I metabotropic glutamate receptors regulates receptor trafficking and signaling. J. Neurosci. 31, 5921-5930.
9. Colbran R. J., (2004) Targeting of calcium/calmodulin-dependent protein kinase II. Biochem. J. 378, 1-16.
10. Colbran R. J., and, Soderling T. R., (1990) Calcium/calmodulin- independent autophosphorylation sites of calcium/calmodulin-dependent protein kinase II. Studies on the effect of phosphorylation of threonine 305/306 and serine 314 on calmodulin binding using synthetic peptides. J. Biol. Chem. 265, 11213-11219.
11. Doherty A. J., Palmer M. J., Bortolotto Z. A., Hargreaves A., Kingston A. E., Ornstein P. L., Schoepp D. D., Lodge D., and, Collingridge G. L., (2000) A novel, competitive mGlu(5) receptor antagonist (LY344545) blocks DHPG-induced potentiation of NMDA responses but not the induction of LTP in rat hippocampal slices. Br. J. Pharmacol. 131, 239-244.
12. Enz R., (2007) The trick of the tail: protein-protein interactions of metabotropic glutamate receptors. BioEssays 29, 60-73.
13. Enz R., (2012) Metabotropic glutamate receptors and interacting proteins: evolving drug targets. Curr. Drug Targets 13, 145-156.
14. Fagni L., (2012) Diversity of metabotropic glutamate receptor-interacting proteins and pathophysiological functions. Adv. Exp. Med. Biol. 970, 63-79.
15. Gardoni F., Caputi A., Cimino M., Pastorino L., Cattabeni F., and, Di Luca M., (1998) Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities. J. Neurochem. 71, 1733-1741.
16. Grishin A. A., Gee C. E., Gerber U., and, Benquet P., (2004) Differential calcium-dependent modulation of NMDA currents in CA1 and CA3 hippocampal pyramidal cells. J. Neurosci. 24, 350-355.
17. Guo M. L., Fibuch E. E., Liu X. Y., Choe E. S., Buch S., Mao L. M., and, Wang J. Q., (2010) CaMKIIα interacts with M4 muscarinic receptors to control receptor and psychomotor function. EMBO J. 29, 2070-2081.
18. Heidinger V., Manzerra P., Wang X. Q., Strasser U., Yu S. P., Choi D. W., and, Behrens M. M., (2002) Metabotropic glutamate receptor 1-induced upregulation of NMDA receptor current: mediation through the Pyk2/Src-family kinase pathway in cortical neurons. J. Neurosci. 22, 5452-5461.
19. Huang H., and, van den Pol A. N., (2007) Rapid direct excitation and long-lasing enhancement of NMDA response by group I metabotropic glutamate receptor activation of hypothalamic melanin-concentrating hormone neurons. J. Neurosci. 27, 11560-11572.
20. Ireland D. R., and, Abraham W. C., (2009) Mechanisms of group I mGluR-dependent long-term depression of NMDA receptor-mediated transmission at schaffer collateral-CA1 synapses. J. Neurophysiol. 101, 1375-1385.
21. Jin D. Z., Guo M. L., Xue B., Fibuch E. E., Choe E. S., Mao L. M., and, Wang J. Q., (2013) Phosphorylation and feedback regulation of metabotropic glutamate receptor 1 by CaMKII. J. Neurosci. 33, 3402-3412.
22. 2+/calmodulin-dependent protein kinase. Proc. Natl Acad. Sci. USA 81, 945-949.
23. Kerner J. A., Standaert D. G., Penney J. B. Jr, Young A. B., and, Landwehrmeyer G. B., (1997) Expression of group I metabotropic glutamate receptor subunit mRNAs in neurochemically identified neurons in the rat neostriatum, neocortex, and hippocampus. Mol. Brain Res. 48, 259-269.
24. Kotecha S. A., Jackson M. F., Al-Mahrouki A., Roder J. C., Orser B. A., and, MacDonald J. F., (2003) Co-stimulation of mGluR5 and N-methyl-D-aspartate receptors is required for potentiation of excitatory synaptic transmission in hippocampal neurons. J. Biol. Chem. 278, 27742-27749.
25. Kuwajima M., Hall R. A., Aiba A., and, Smith Y., (2004) Subcellular and subsynaptic localization of group I metabotropic glutamate receptors in the monkey subthalamic nucleus. J. Comp. Neurol. 474, 589-602.
26. Lee J. H., Lee J., Choi K. Y., et al,. (2008) Calmodulin dynamically regulates the trafficking of the metabotropic glutamate receptor mGluR5. Proc. Natl Acad. Sci. USA 105, 12575-12580.
27. Leonard A. S., Lim I. A., Hemsworth D. E., Horne M. C., and, Hell J. W., (1999) Calcium/calmodulin-dependent protein kinase II is associated with the N-methyl-D-aspartate receptor. Proc. Natl Acad. Sci. USA 96, 3239-3244.
28. Liao G. Y., Wagner D. A., Hsu M. H., and, Leonard J. P., (2001) Evidence for direct protein kinase-C mediated modulation of N-methyl-D-aspartate receptor current. Mol. Pharmacol. 59, 960-964.
29. Liu X. Y., Mao L. M., Zhang G. C., Papasian C. J., Fibuch E. E., Lan H. X., Zhou H. F., Xu M., and, Wang J. Q., (2009) Activity-dependent modulation of limbic dopamine D3 receptors by CaMKII. Neuron 61, 425-438.
30. Lujan R., Nusser Z., Roberts J. D., Shigemoto R., and, Somogyi P., (1996) Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur. J. Neurosci. 8, 1488-1500.
31. Mannaioni G., Marino M. J., Valenti O., Traynelis S. F., and, Conn P. J., (2001) Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J. Neurosci. 21, 5925-5934.
32. Mao L. M., Guo M. L., Jin D. Z., Fibuch E. E., Choe E. S., and, Wang J. Q., (2011) Posttranslational modification biology of glutamate receptors and drug addiction. Front. Neuroanat. 5, 19.
33. Minakami R., Jinnai N., and, Sugiyama H., (1997) Phosphorylation and calmodulin binding of the metabotropic glutamate receptor subtype 5 (mGluR5) are antagonistic in vitro. J. Biol. Chem. 272, 20291-20298.
34. Mockett B. G., Guevremont D., Wutte M., Hulme S. R., Williams J. M., and, Abraham W. C., (2011) Calcium/calmodulin-dependent protein kinase II mediates group I metabotropic glutamate receptor-dependent protein synthesis and long-term depression in rat hippocampus. J. Neurosci. 31, 7380-7391.
35. Niswende C. M., and, Conn P. J., (2010) Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu. Rev. Pharmacol. Toxicol. 50, 295-322.
36. Omkumar R. V., Kiely M. J., Rosenstein A. J., Min K. T., and, Kennedy M. B., (1996) Identification of a phosphorylation site for calcium/calmodulin- dependent protein kinase II in the NR2B subunit of the N-methyl-D-aspartate receptor. J. Biol. Chem. 271, 31670-31678.
37. Petralia R. S., (2012) Distribution of extrasynaptic NMDA receptors on neurons. ScientificWorldJournal 2012, 267120.
38. Pisani A., Calabresi P., Centonze D., and, Bernardi G., (1997) Enhancement of NMDA responses by group I metabotropic glutamate receptor activation in striatal neurons. Br. J. Pharmacol. 120, 1007-1014.
39. Pisani A., Bernardi G., Bonsi P., Centonze D., Giacomini P., and, Calabresi P., (2000) Cell-type specificity of mGluR activation in striatal neuronal subtypes. Amino Acids 19, 119-129.
40. Pisani A., Gubellini P., Bonsi P., Conquet F., Picconi B., Centonze D., Barnardi G., and, Calabresi P., (2001) Metabotropic glutamate receptor 5 mediates the potentiation of N-methyl-D-aspartate responses in medium spiny striatal neurons. Neuroscience 106, 579-587.
41. Rosenbrock H., Kramer G., Hobson S., Koros E., Grundl M., Grauert M., Reymann K. G., and, Schroder U. H., (2010) Functional interaction of metabotropic glutamate receptor 5 and NMDA-receptor by a metabotropic glutamate receptor 5 positive allosteric modulator. Eur. J. Pharmacol. 639, 40-46.
42. Skeberdis V. A., Lan J., Opitz T., Zheng X., Bennett M. V., and, Zukin R. S., (2001) mGluR1-mediated potentiation of NMDA receptors involves a rise in intracellular calcium and activation of protein kinase C. Neuropharmacology 40, 856-865.
43. Strack S., and, Colbran R. J., (1998) Autophosphorylation-dependent targeting of calcium/calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl-D-aspartate receptor. J. Biol. Chem. 273, 20689-20692.
44. Strack S., McNeill R. B., and, Colbran R. J., (2000) Mechanism and regulation of calcium/calmodulin-dependent protein kinase II targeting to the NR2B subunit of the N-methyl-D-aspartate receptor. J. Biol. Chem. 275, 23798-23806.
45. Tallaksen-Greene S. J., Kaatz K. W., Romano C., and, Albin R. L., (1998) Localization of mGluR1a-like immunoreactivity and mGluR5a-like immunoreactivity in identified population of striatal neurons. Brain Res. 780, 210-217.
46. Testa C. M., Standaert D. G., Young A. B., and, Penney J. B. Jr, (1994) Metabotropic glutamate receptor mRNA expression in the basal ganglia of the rat. J. Neurosci. 14, 3005-3018.
47. Testa C. M., Standaert D. G., Landwehrmeyer G. B., Penney J. B. Jr, and, Young A. B., (1995) Differential expression of mGluR5 metabotropic glutamate receptor mRNA by rat striatal neurons. J. Comp. Neurol. 354, 241-252.
48. Traynelis S. F., Wollmuth L. P., McBain C. J., Menniti E. S., Vance K. M., Ogden K. K., Hansen K. B., Yuan H., Myers S. J., and, Dingledine R., (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405-496.
49. Yang K., Takeuchi K., Wei F., Dubner R., and, Ren K., (2011) Activation of group I mGlu receptors contributes to facilitation of NMDA receptor membrane current in spinal dorsal horn neurons after hind paw inflammation in rats. Eur. J. Pharmacol. 670, 509-518.